Original Article
Implementation of a multidisciplinary infectious diseases team in a tertiary hospital within an Antimicrobial Stewardship Program F. M. Buyle1, M. Wallaert2, N. Beck1, J. Boelens3, S. Callens4, G. Claeys3, S. Deryckere1, E. Haegeman1, I. Leroux-Roels3, E. Sermijn4, E. Steel5, H. Robays1, L. Vandekerckhove4, K. Vermis1, D. Vogelaers4 1
Department of Pharmacy, Ghent University Hospital, Belgium, 2Faculty of Pharmaceutical Sciences, Ghent University, Belgium, 3Department of Microbiology, Ghent University Hospital, Belgium, 4Department of General Internal Medicine, Ghent University Hospital, Belgium, 5Department of Haematology, Ghent University Hospital, Belgium
Background: In January 2011, as part of an antimicrobial stewardship program the Antimicrobial Management Team (AMT) at the Ghent University Hospital initiated a multidisciplinary Infectious Diseases Team (MIT) consisting of infectious diseases physicians, clinical microbiologists, and clinical pharmacists. The aim of this study is to describe the type and acceptance rate of recommendations provided by the MIT. Method: Prospective, observational study in a tertiary care, university teaching hospital with 1062 beds in non-consecutive hospitalized adult patients, excluding intensive care units and paediatrics. Results: The MIT communicated 432 recommendations in 87 days observed. Of the 293 patients for whom a recommendation was made, the median age was 57 years (range: 16–91 years) and 169 (57.7%) were male. Skin or soft tissue infections (14%), respiratory tract infections (13%), infections without known focus (11%), abdominal infections (11%), and bone infections (8%) were most common. Recommendations were made to perform additional clinical investigation(s) [N5137 (27%)], to adjust the dose of an antimicrobial drug [N542 (8%)], to stop an antimicrobial drug [N5104 (21%)], to switch from a parenteral to an oral drug [N539 (8%)] or to initiate an antimicrobial drug [N5178 (36%)], with an acceptance rate of 73.0%, 83.3%, 81.7%, 76.9%, and 84.0%, respectively. Conclusions: The MIT formulated about five recommendations a day primarily focusing on pharmacotherapy, but also on clinical investigations. In both fields, a high acceptance rate was observed. Keywords: Antimicrobial stewardship program, Antibiotic prescribing, Intervention strategy, Implementation
Background Antimicrobial stewardship refers to coordinated interventions designed to improve and measure the appropriate use of antimicrobial agents by promoting the selection of the optimal antimicrobial drug regimen including dosing, duration of therapy, and route of administration.1 The major objectives are to optimize the clinical outcomes related to antimicrobial use while minimizing toxicity and other adverse events and limiting the selective pressure on bacterial populations that drives the emergence of antimicrobial-resistant strains. Infections caused by multidrug-resistant bacteria are associated with higher mortality, prolonged
Correspondence to: F. M. Buyle, Department of Pharmacy, Ghent University Hospital, De Pintelaan, 185, 9000 Ghent, Belgium. Email: [email protected]
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hospital stay, and increased costs.2 The emergence of multidrug-resistant organisms limits therapeutic choices in hospital-acquired infections. Reducing and preventing antimicrobial resistance by enhancing the appropriate use of antimicrobials is one of the cornerstones of the European Union policy against antimicrobial resistance.3 Antibiotic stewardship programs are proposed as a tool to optimize the prescribing of antibiotics.4 Antimicrobial stewardship may also reduce excessive costs attributable to suboptimal antimicrobial use.1 A recent study has shown that 38% of the antibiotic usage in European hospitals was not compliant to guidelines which need to be promoted through an antimicrobial stewardship program.5 To influence the antimicrobial prescribing behaviour, a multidisciplinary approach which involves opinion leaders and senior clinicians is preferable.
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Ideally, such a multidisciplinary antimicrobial stewardship team should bring different competences together, including infectious diseases (ID) physicians, clinical microbiologists, and clinical pharmacists. Since 2002, the Belgian Antibiotic Policy Coordination Committee was able to secure federal funding, provide technical guidance, and offer advanced specialist training for the formal establishment and follow-up of Antimicrobial Management Teams (AMTs) in Belgian hospitals.6 The minimal composition, mandate, and tasks of hospital AMTs have been consolidated in legislation (Royal Decree of 12 February 2008) on the norms for AMTs as dedicated subgroups of the hospital Drugs and Therapeutic Committee.6 The AMT of the Ghent University hospital provides national (The Sanford Guide To Antimicrobial Therapy — Belgian/Luxembourg Edition) and local antimicrobial guidelines to the prescribers.7 The electronic medical record allows physicians to consult the microbiological results of the clinical laboratory, including identification and susceptibility of pathogens. Eighty per cent of the wards use a computerised physician order entry (CPOE) system in which dosing regimens are incorporated in medication order sets and where current and past antimicrobial therapies can be consulted. Wards where CPOE is not yet implemented can prescribe restricted antimicrobials (voriconazol, caspofungin, anidulafungin, liposomal amphotericin B, meropenem, piperacillin/tazobactam, linezolid, tigecycline,
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vancomycin, teicoplanin, colimycin, ceftazidim, levofloxacin, moxifloxacin, ciprofloxacin) with a specific antibiotic prescription form. The AMT at our hospital initiated a multidisciplinary infectious diseases team (MIT) in January 2011, as part of an antimicrobial stewardship program, which is directed by ID physicians and also consists of clinical microbiologists and clinical pharmacists. Once a week, a haematologist joins the team. Figure 1 gives a schematic representation of the activities of the MIT. The MIT meets daily to discuss (1) requests for ID consultations reviewed by ID physicians; (2) positive blood cultures and cultures with resistant strains or with organisms requiring special attention, reviewed by microbiologists; and (3) presumed inappropriate therapies identified by pharmacists. The pharmacists review therapies with antifungals, meropenem, piperacillin/tazobactam, linezolid, tigecycline, vancomycin and teicoplanin, blood concentrations of antimicrobials requiring monitoring (vancomycin and teicoplanin, aminoglycosides,voriconazole), and antimicrobials with high bioavailability that may be switched from parenteral to oral administration based on the electronic medical patient record. The MIT communicates its recommendations to the physicians by phone and by notes in the electronic patient file where a specific MIT section is available. The MIT limits its interventions to adult patients hospitalized in non-critical care departments. Critical care patients are discussed weekly in a separate meeting with clinical
Figure 1 Flowchart activities multidisciplinary infectious diseases team.
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microbiologists and intensive care physicians. The pediatric department has a dedicated pediatric ID physician. The aim of this pilot study is to describe the type and acceptance rate of interventions provided by the MIT.
Methods A prospective, observational study was performed in a tertiary care, teaching hospital with 1062 beds. The MIT pharmacists registered every recommendation communicated by the MIT during 87 nonconsecutive days between October 2011 and May 2012. The following data were registered in a standardised case record form: date of MIT recommendation, hospitalisation ward, type of infection, and current antimicrobial treatment. Five types of recommendations can be distinguished: (1) initiating or changing an antimicrobial regimen; (2) additional
clinical investigations; (3) dosing adjustments; (4) switching from parenteral to oral formulations; and (5) discontinuing antimicrobials. The rationale for the recommendations and the specific antimicrobials involved were registered. Recommendations were scored as accepted when a physician implemented the recommendation(s) within 3 days after the communication. The acceptance rate was classified as ‘not documented’ in those cases where it was not possible to document this retrospectively (e.g. patient discharged or transferred to another health-care facility). The study was approved by the local Ethics Committee.
Results The MIT communicated 432 recommendations during 87 non-consecutive days in 293 patients The median age was 57 years (range: 16–91 years) and 169 (57.7%) were male.
Table 1 Classification of the recommendations provided by the MIT with acceptance rates
Classification of recommendation
Number of recommendations Accepted N (%) N (%)
Acceptance Not not documented accepted N (%) N (%)
(A) Additional clinical investigation Type of investigation Other* Microbiological culture CT scan Standard RX scan Therapeutic drug monitoring Standard echography Transoesophageal echography ID consultation Transthoracic echocardiography (B) Dosing adjustment Reason Subtherapeutic or toxic serum concentration Evidence-based guidelines Other{ renal impairment Type of adjustment Increase Reduction Same daily dose, other dosing regimen (C) Stop antimicrobial therapy Reason No indication to proceed Prolonged therapy Tentative (D) Switch parenteral to oral (E) Initiation antimicrobial therapy Reason Replacement Narrow spectrum Effectiveness Broaden spectrum Oral alternative Less side effects Addition Effectiveness Broaden spectrum Restart Reason unknown
137 (27%) 80 (58%) 43 (31%) 20 (15%) 13 (9%) 11 (8%) 9 (7%) 9 (7%) 8 (6%) 1 (1%) 42 (8%) 15 (36%) 15 (36%) 8 (19%) 4 (10%) 22 (52%) 11 (26%) 9 (21%) 104 (21%) 70 (67%) 25 (24%) 9 (9%) 39 (8%) 178 (36%) 113 (63%) 38 (34%) 30 (27%) 20 (18%) 19 (17%) 13 (12%) 26 (15%) 13 (50%) 13 (50%) 2 (1%) 2 (1%)
5 (4%) 2 (3%) 0 (0%) 1 (5%) 0 (0%) 0 (0%) 0 (0%) 2 (22%) 0 (0%) 0 (0%) 3 (7%) 0 (0%) 2 (13%) 1 (13%) 0 (0%) 2 (9%) 0 (0%) 1 (11%) 4 (4%) 4 (6%) 0 (0%) 0 (0%) 1 (3%) 11 (6%) 7 (6%) 1 (3%) 2 (7%) 1 (5%) 1 (5%) 1 (8%) 1 (4%) 0 (0%) 1 (8%) 0 (0%) 0 (0%)
100 (73%) 62 (78%) 32 (74%) 14 (70%) 10 (77%) 9 (82%) 6 (67%) 7 (78%) 5 (63%) 1 (100%) 35 (83%) 12 (80%) 12 (80%) 7 (88%) 4 (100%) 16 (73%) 11 (100%) 8 (89%) 85 (82%) 57 (81%) 22 (88%) 6 (67%) 30 (77%) 150 (84%) 94 (83%) 32 (84%) 26 (87%) 15 (75%) 17 (89%) 10 (77%) 23 (88%) 12 (92%) 11 (85%) 1 (50%) 2 (100%)
32 (2%) 16 (20%) 11 (26%) 5 (25%) 3 (23%) 2 (18%) 3 (33%) 0 (0%) 3 (38%) 0 (0%) 4 (10%) 3 (20%) 1 (7%) 0 (0%) 0 (0%) 4 (18%) 0 (0%) 0 (0%) 15 (14%) 9 (13%) 3 (12%) 3 (33%) 8 (21%) 17 (10%) 12 (11%) 5 (13%) 2 (7%) 4 (20%) 1 (5%) 2 (15%) 2 (8%) 1 (8%) 1 (8%) 1 (50%) 0 (0%)
Note: *Procalcitonin measurement (12 recommendations); nuclear magnetic resonance scan (6); bronchoalveolar lavage (4); polymerase chain reaction analysis (4); positron emission tomography (3), etc. { Different length of administration, increase of dose for penetration into sternum bone, increase of dose because of intermediate sensitivity of bacterial strain, increase of dose because of infection of vascular prosthesis, different dosing regimens because of parenteral administration in home setting, increase of dose because of high body weight, tentative.
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Skin or soft tissue infections (14%), respiratory tract infections (13%), infections without known focus (11%), abdominal infections (11%), and bone and joint infections, including prosthetic infections (8%), were most frequently involved. In 277 (64.1%) of the recommendations, the MIT proposed a modification in therapy or further clinical investigations which were accepted. In 84 (19.4%) of the recommendations, the MIT suggested to continue the actual therapy which was implemented. This resulted in a total acceptance rate of 83.5%. For the other recommendations, 57 (13.2%) were not implemented and for 14 (3.2%) implementation could not be documented. MIT recommendations originated from new electronically requested ID consultations (61%), current antimicrobial therapies provided by pharmacists (18%), follow-up of earlier requested ID consultations (12%), microbiological information provided by microbiologists (4%), current therapies provided by ID physicians (3%), and haematologists (2%). The electronic ID consultations were ordered by 30 medical disciplines, ranging from 1 to 24 (median: 7.5) requests per discipline. The majority of the recommendations were made for patients on the following wards: abdominal surgery (16.2%), gastroenterology (9.3%), thoracovascular surgery (7.9%), rehabilitation medicine (5.8%), and orthopaedics (5.0%). Some of the 432 recommendations consisted of multiple types of recommendations, which were taken into account individually in Table 1. This resulted in 500 individual recommendations. Recommendations were made to perform additional clinical investigation(s) [N5137 (27%)], to adjust a dose of an antimicrobial drug [N542 (8%)], to stop an antimicrobial drug [N5104 (21%)], to switch from a parenteral to an oral drug [N539 (8%)] and to initiate an antimicrobial drug [N5178 (36%)], with an acceptation rate of respectively 73.0%, 83.3%, 81.7%, 76.9%, and 84.0% (Table 1). Of the 178 initiated antimicrobials, 113 (63%) were a replacement of and 26 (15%) an addition to the current therapy. Within the accepted recommendations, vancomycin, piperacillin/tazobactam, and meropenem treatments were more frequently stopped versus initiated (respectively 31 versus 5, 21 versus 7, and 20 versus 14). Considering the administration route, parenteral therapies were more frequently stopped than initiated (148 versus 97). In general, treatments were more frequently discontinued instead of initiated (184 versus 152) after a MIT recommendation. This is not a likelihood but a frequency distribution as recommendations to continue treatments were more likely to be implemented.
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Discussion This study shows that an average of five recommendations per day was provided by the MIT, of which 83% were accepted. This acceptance rate is comparable with numbers in similar studies performed in the USA, Brazil, Singapore, and Australia, showing acceptance rates ranging from 64% to 80%.8–12 Remarkably, the number of recommendations seems slightly higher in our study. This could be the result of the inclusion of pharmacotherapeutic, as well as diagnostic recommendations, in contrast to the previously published reports. In the other studies, the AMT program was performed by ID physicians, together with clinical pharmacists, whereas only in one study, there was also participation of a clinical microbiologist (9). The numbers of beds ranged from 60 to 1596.8–12 Our recommendations cover a wide range of infection types, with a majority of skin or soft tissue infections, respiratory tract infections, infections without known focus, and abdominal infections. Some of these infections can be complicated and complex, requiring a long duration of therapy, a setting in which the advice of the MIT can be important. The majority (61%) of the recommendations originate from ID consultations. This may reflect the embedment of this clinical service within the hospital. A significant number (18%) of recommendations originate from therapies reviewed by clinical pharmacists. Pharmacists spend approximately 2 hours per day in analysing treatments with antifungals (with the exception of fluconazole), meropenem, piperacillin/ tazobactam, linezolid, tigecycline, vancomycin, teicoplanin, and antimicrobials with a high bioavailability that may be switched from parenteral to oral administration. Because this represents a significant workload each type of antimicrobial agent is reviewed only once a week. Data-mining software able to generate automated reports based on pharmaceutical, clinical, and microbiological data could have a time-saving effect.11 This should allow us to enhance the frequency of the actual antimicrobial agents and to evaluate additional antimicrobial agents. Furthermore, computer decision support systems could support physicians upon the initiation of a therapy.13,14 Such a system is already applied on the intensive care unit of our hospital.14 However, this was outside the scope of the current study. The number of recommendations originating from positive microbiological cultures provided by clinical microbiologists is small, because during the time period of the study, most of the positive cultures were directly discussed by the clinical microbiologists with the treating physicians outside the framework of the MIT. This is a direct consequence of the different
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organisation of the microbiology laboratory, where the results are generated early in the morning, in contrast with the MIT meetings which are held in the late afternoon. The majority (73%) of the recommendations focus on pharmacotherapy. All recommendations to reduce the dose of antimicrobials were accepted, while recommendations to increase the dose had a lower acceptance rate. Physicians seem to feel more confident with reducing doses considering compromised renal function or risk of side effects. They may not yet be fully aware of the concept of individualised antimicrobial therapy. This may require increasing doses, e.g. in infections with less sensitive strains, in patients with significant pharmacokinetic changes, such as increased distribution volume (burns, cirrhosis) or the phenomenon of augmented renal clearance in critically ill.15 Recommendations that propose a tentative stop of an antimicrobial therapy and an observation of the clinical evolution imply a greater degree of uncertainty for physicians which can explain the low acceptance rate in this setting. The acceptance rate to switch from a parenteral to an oral formulation (IV–PO switch) of the same antimicrobial is relatively low. An explanation could be that pharmacists’ only source to consider possible switches is the electronic medical record where clinical data that could support the medical decision to continue parenteral therapy (e.g. severe vomiting, diarrhea, not functional tube) were not always documented. The proportion of recommendations proposing an IV–PO switch is small, which could be the result of other and earlier initiatives towards physicians. Within the same hospital, we have reported high compliance with internal guidelines on IV–PO switch.16,17 These initiatives were developed outside the framework of the MIT, but were coordinated by the AMT. Recommendations to initiate an antimicrobial therapy have the highest overall acceptance rate with physicians. Most recommendations in this category propose to replace a current antimicrobial by an alternative. Most persuasive reasons to initiate an antimicrobial therapy were to enhance effectiveness, to narrow spectrum, and to allow a switch to oral therapy. The analysis of accepted recommendations suggests that the MIT was able to de-escalate therapies, to switch to oral antimicrobials, and to discontinue antimicrobials when applicable. About 17% of the recommendations focus on additional clinical investigations with an acceptance rate of 73%, which is lower compared to pharmacotherapy oriented recommendations, but comparable with a recently published similar study.18 The lower acceptance rate on diagnostic issues suggests that physicians more readily accept recommendations
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on pharmacotherapy as compared to critical reflections on their diagnostic path. This is also shown by the low uptake of performing transesophageal echocardiography in patients with Staphylococcus aureus bacteraemia. As a result of these data, patients with a Staphylococcus aureus bacteraemia are now prospectively followed during their hospital stay to ensure echocardiography screening for latent infective endocarditis.19 Establishing a culture of measurement and clinician feedback is an effective stewardship strategy.4,20 The effectiveness can be improved by the Feedback Intervention Theory through providing specific, frequent, and written suggestions for improvement.21 This was also applied by the MIT by documenting recommendations in the CPOE system and by additional communication by phone. Another strength of the MIT is that follow-up by the MIT is provided for patients with complex infections. This is strongly appreciated by the physicians. The multidisciplinary composition of the MIT reflects the recommendations in the literature.2,4,22 The MIT is directed by an infectious disease physician who is a respected authority which is a fundamental feature in marketing the MIT concept.23 Initially, the pharmacist reviewed only prolonged therapies (.10 days) of the target antimicrobial agents, which have changed over time to all treatments. Pre-authorization of restricted antimicrobial agents is not implemented in our hospital and only once a week, each type of antimicrobial agents is reviewed. The combination of these two factors indicates potential for further optimization. This will increase the workload, which can be in turn reduced by implementing automated reports. One study from a hospital in the USA with 513 beds described that software-generated antimicrobial therapy reports contain information on approximately 60–80 patient cases, resulting in about 20 cases daily after evaluation by a pharmacist. These cases are then reviewed together with an ID physician. Projecting this method to our hospital, this could generate 36 cases on a daily basis to discuss within the MIT.11 In order to support physicians during the diagnostic evaluation of the patient, some guidelines are now linked to the data of clinical chemistry (e.g. serum concentration levels of glycopeptide and aminoglycoside agents are linked to drug therapeutic monitoring guidelines) and microbiology (positive blood cultures with Staphylococcus aureus are linked to the Staphylococcus aureus bacteremia guideline). This pilot study has some limitations. Reasons to decline a recommendation were not assessed. Recent literature on antimicrobial stewardship focuses on the behaviour of individual prescribers. This could lead to understanding the barriers to and facilitators of
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behavioural change.24 This should be taken into account for further research. No statements can be made on the cost-effectiveness, patient safety, impact on morbidity, and mortality and local resistance patterns. Restricted antibiotics (e.g. vancomycin, piperacillin-tazobactam, and meropenem) were more frequently stopped than initiated and oral therapies were more frequently initiated compared with parenteral therapy. This suggests that the MIT can have a positive impact on antimicrobial expenditure. In the past, this was shown in our hospital for an IV–PO switch program.16 This is in line with documented positive impact of antimicrobial stewardship programs on antimicrobial expenditure and clinical outcome.8–12,25
Conclusion This prospective observational pilot study showed that the multidisciplinary infectious diseases team, as part of an antimicrobial stewardship program, formulated about five interventions a day for noncritically ill adult patients. Recommendations were communicated by phone and by notes in the electronic patient file resulting in high acceptance rates. Acceptance rates were higher for recommendations on pharmacotherapy as compared to diagnostic issues.
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Disclaimer Statements Funding None to declare.
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Conflicts of interest The authors declare that they have no conflict of interest.
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Ethics approval The study was approved by the local Ethics Committee.
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Acknowledgements We acknowledge the trainee hospital pharmacists Nele Clottens (PharmD), Ilse Vanlerberghe (PharmD), Mieke Van Tomme (PharmD), and the trainee infectious disease physicians Filip Moerman (MD), Sarah Temmerman (MD), and Bart Werbrouck (MD) for their contributions in the MIT activities. We acknowledge hospital pharmacist Annemie Somers (PharmD, PhD) for the critical remarks in analysing the data.
References 1 Society for Healthcare Epidemiology of America; Infectious Diseases Society of America; Pediatric Infectious Diseases Society. Policy Statement on Antimicrobial Stewardship by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), and the Pediatric Infectious Diseases Society (PIDS) Society for Healthcare Epidemiology of America; Infectious Diseases Society of America; Pediatric Infectious Diseases Society. Infect Control Hosp Epidemiol. 2012;33:322–7. 2 Davey P, Brown E, Charani E, Fenelon L, Gould IM, Holmes A, et al. Interventions to improve antibiotic prescribing
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practices for hospital inpatients. Cochrane Database Syst Rev. 2013;(4):CD003543. Communication from the commission to the European Parliament and the council. Action plan against the rising threats from Antimicrobial Resistance Brussels. Brussels: European Commission; 2011 [cited 2013 Jun 28]. Available from: http://ec.europa.eu/dgs/health_consumer/docs/communication_amr_2011_748_en.pdf Dellit TH, Owens RC, McGowan JE, Gerding DN, Weinstein RA, Burke JP, et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis. 2007;44:159–77. Zarb P, Amadeo B, Muller A, Drapier N, Vankerckhoven V, Davey P, et al. Identification of targets for quality improvement in antimicrobial prescribing: the web-based ESAC Point Prevalence Survey 2009. J Antimicrob Chemother. 2011;66:443–9. van Gastel E, Costers M, Peetermans WE, Struelens MJ, and on behalf of the Hospital Medicine Working Group of the Belgian Antibiotic Policy Coordination Committee. Nationwide implementation of antibiotic management teams in Belgian hospitals: a self-reporting survey. J Antimicrob Chemother. 2010;65:576–80. Sanford JP, Gilbert DN, Chambers HF, Eliopoulos GM, Moellering RC, Saag MS. The Sanford guide to antimicrobial therapy, 2012–2013. 23rd ed. Belgian/Luxembourg version. Sperryville, VA: Belgian/Luxembourg Working Party on Antimicrobial Therapy; 2013. Pate PG, Storey DF, Baum DL. Implementation of an antimicrobial stewardship program at a 60-bed long-term acute care hospital. Infect Control Hosp Epidemiol. 2012;33:405–8. Liew YX, Lee W, Loh JC, Cai Y, Tang SS, Lim CL, et al. Impact of an antimicrobial stewardship programme on patient safety in Singapore General Hospital. Int J Antimicrob Agents. 2012;40:55–60. Magedanz L, Silliprandi EM, dos Santos R. Impact of the pharmacist on a multidisciplinary team in an antimicrobial stewardship program: a quasi-experimental study. Int J Clin Pharm. 2012;34:290–4. Nowak M, Nelson R, Breidenbach J. Clinical and economic outcomes of a prospective antimicrobial stewardship program. Am J Health-Syst Pharm. 2012;69:1500–8. Cairns KA, Jenney AW, Abbott IJ, Skinner MJ, Doyle JS, Dooley M, et al. Prescribing trends before and after implementation of an antimicrobial stewardship program. Med J Aust. 2013;18:262–6. Pestotnik SL. Expert Clinical Decision Support Systems to Enhance Antimicrobial Stewardship Programs: insights from the society of infectious diseases pharmacists. Pharmacotherapy. 2005;25:1116–25. Steurbaut K, Colpaert K, Gadeyne B, Depuydt P, Vosters P, Danneels C, et al. COSARA: integrated service platform for infection surveillance and antibiotic management in the ICU. J Med Syst. 2012;36:3765–75. Udy AA, Roberts JA, de Waele JJ, Paterson DL, Lipman J. What’s behind the failure of emerging antibiotics in the critically ill? Understanding the impact of altered pharmacokinetics and augmented renal clearance. Int J Antimicrob Agents. 2012;39:455–7. Buyle F, Vogelaers D, Peleman R, van Maele G, Robays H. Implementation of guidelines for sequential therapy with fluoroquinolones in a Belgian hospital. Pharm World Sci. 2010;32:404–10. Buyle FM, Metz-Gercek S, Mechtler R, Kern WV, Robays H, Vogelaers D, et al.; Antibiotic Strategy International-ABS Quality Indicators Team. Prospective multicentre feasibility study of a quality of care indicator for intravenous to oral switch therapy with highly bioavailable antibiotics. J Antimicrob Chemother. 2012;67:2043–6. Teo J, Kwa AL, Loh J, Chlebicki MP, Lee W. The effect of a whole-system approach in an antimicrobial stewardship programme at the Singapore General Hospital. Eur J Clin Microbiol Infect Dis. 2012;31:947–55. Kern WV, Metz-Gercek S, Buyle F, Jindrak V, Lechner A, Mittermayer H, et al. Staphylococcus aureus bloodstream infection management indicators as quality indicators for hospital antibiotic stewardship: feasibility study by the ABS International Quality Indicators (ABS QI) team. Clin Microbiol Infect. 2009;15(Suppl 4):S188. Malcolm W, Nathwani D, Davey P, Cromwell T, Patton A, Reilly J, et al. From intermittent antibiotic point prevalence
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23 Redelmeier DA, Cialdini B. Problems for clinical judgement: 5. Principles of influence in medical practice. Can Med Assoc J. 2002;166:1680–4. 24 Charani E, Edwards R, Sevdalis N, Alexandrou B, Sibley E, Mullett D, et al. Behavior change strategies to influence antimicrobial prescribing in acute care: a systematic review. Clin Infect Dis. 2011;53:651–62. 25 Dryden M, Saeed K, Townsend R, Winnard C, Bourne1 S, Parker N. Antibiotic stewardship and early discharge from hospital: impact of a structured approach to antimicrobial management. J Antimicrob Chemother. 2012;67:2289–96.
Implementation of a multidisciplinary infectious diseases team in a tertiary hospital within an Antimicrobial Stewardship Program F. M. Buyle1, M. Wallaert2, N. Beck1, J. Boelens3, S. Callens4, G. Claeys3, S. Deryckere1, E. Haegeman1, I. Leroux-Roels3, E. Sermijn4, E. Steel5, H. Robays1, L. Vandekerckhove4, K. Vermis1, D. Vogelaers4 1
Department of Pharmacy, Ghent University Hospital, Belgium, 2Faculty of Pharmaceutical Sciences, Ghent University, Belgium, 3Department of Microbiology, Ghent University Hospital, Belgium, 4Department of General Internal Medicine, Ghent University Hospital, Belgium, 5Department of Haematology, Ghent University Hospital, Belgium
Background: In January 2011, as part of an antimicrobial stewardship program the Antimicrobial Management Team (AMT) at the Ghent University Hospital initiated a multidisciplinary Infectious Diseases Team (MIT) consisting of infectious diseases physicians, clinical microbiologists, and clinical pharmacists. The aim of this study is to describe the type and acceptance rate of recommendations provided by the MIT. Method: Prospective, observational study in a tertiary care, university teaching hospital with 1062 beds in non-consecutive hospitalized adult patients, excluding intensive care units and paediatrics. Results: The MIT communicated 432 recommendations in 87 days observed. Of the 293 patients for whom a recommendation was made, the median age was 57 years (range: 16–91 years) and 169 (57.7%) were male. Skin or soft tissue infections (14%), respiratory tract infections (13%), infections without known focus (11%), abdominal infections (11%), and bone infections (8%) were most common. Recommendations were made to perform additional clinical investigation(s) [N5137 (27%)], to adjust the dose of an antimicrobial drug [N542 (8%)], to stop an antimicrobial drug [N5104 (21%)], to switch from a parenteral to an oral drug [N539 (8%)] or to initiate an antimicrobial drug [N5178 (36%)], with an acceptance rate of 73.0%, 83.3%, 81.7%, 76.9%, and 84.0%, respectively. Conclusions: The MIT formulated about five recommendations a day primarily focusing on pharmacotherapy, but also on clinical investigations. In both fields, a high acceptance rate was observed. Keywords: Antimicrobial stewardship program, Antibiotic prescribing, Intervention strategy, Implementation
Background Antimicrobial stewardship refers to coordinated interventions designed to improve and measure the appropriate use of antimicrobial agents by promoting the selection of the optimal antimicrobial drug regimen including dosing, duration of therapy, and route of administration.1 The major objectives are to optimize the clinical outcomes related to antimicrobial use while minimizing toxicity and other adverse events and limiting the selective pressure on bacterial populations that drives the emergence of antimicrobial-resistant strains. Infections caused by multidrug-resistant bacteria are associated with higher mortality, prolonged
Correspondence to: F. M. Buyle, Department of Pharmacy, Ghent University Hospital, De Pintelaan, 185, 9000 Ghent, Belgium. Email: [email protected]
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hospital stay, and increased costs.2 The emergence of multidrug-resistant organisms limits therapeutic choices in hospital-acquired infections. Reducing and preventing antimicrobial resistance by enhancing the appropriate use of antimicrobials is one of the cornerstones of the European Union policy against antimicrobial resistance.3 Antibiotic stewardship programs are proposed as a tool to optimize the prescribing of antibiotics.4 Antimicrobial stewardship may also reduce excessive costs attributable to suboptimal antimicrobial use.1 A recent study has shown that 38% of the antibiotic usage in European hospitals was not compliant to guidelines which need to be promoted through an antimicrobial stewardship program.5 To influence the antimicrobial prescribing behaviour, a multidisciplinary approach which involves opinion leaders and senior clinicians is preferable.
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Ideally, such a multidisciplinary antimicrobial stewardship team should bring different competences together, including infectious diseases (ID) physicians, clinical microbiologists, and clinical pharmacists. Since 2002, the Belgian Antibiotic Policy Coordination Committee was able to secure federal funding, provide technical guidance, and offer advanced specialist training for the formal establishment and follow-up of Antimicrobial Management Teams (AMTs) in Belgian hospitals.6 The minimal composition, mandate, and tasks of hospital AMTs have been consolidated in legislation (Royal Decree of 12 February 2008) on the norms for AMTs as dedicated subgroups of the hospital Drugs and Therapeutic Committee.6 The AMT of the Ghent University hospital provides national (The Sanford Guide To Antimicrobial Therapy — Belgian/Luxembourg Edition) and local antimicrobial guidelines to the prescribers.7 The electronic medical record allows physicians to consult the microbiological results of the clinical laboratory, including identification and susceptibility of pathogens. Eighty per cent of the wards use a computerised physician order entry (CPOE) system in which dosing regimens are incorporated in medication order sets and where current and past antimicrobial therapies can be consulted. Wards where CPOE is not yet implemented can prescribe restricted antimicrobials (voriconazol, caspofungin, anidulafungin, liposomal amphotericin B, meropenem, piperacillin/tazobactam, linezolid, tigecycline,
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vancomycin, teicoplanin, colimycin, ceftazidim, levofloxacin, moxifloxacin, ciprofloxacin) with a specific antibiotic prescription form. The AMT at our hospital initiated a multidisciplinary infectious diseases team (MIT) in January 2011, as part of an antimicrobial stewardship program, which is directed by ID physicians and also consists of clinical microbiologists and clinical pharmacists. Once a week, a haematologist joins the team. Figure 1 gives a schematic representation of the activities of the MIT. The MIT meets daily to discuss (1) requests for ID consultations reviewed by ID physicians; (2) positive blood cultures and cultures with resistant strains or with organisms requiring special attention, reviewed by microbiologists; and (3) presumed inappropriate therapies identified by pharmacists. The pharmacists review therapies with antifungals, meropenem, piperacillin/tazobactam, linezolid, tigecycline, vancomycin and teicoplanin, blood concentrations of antimicrobials requiring monitoring (vancomycin and teicoplanin, aminoglycosides,voriconazole), and antimicrobials with high bioavailability that may be switched from parenteral to oral administration based on the electronic medical patient record. The MIT communicates its recommendations to the physicians by phone and by notes in the electronic patient file where a specific MIT section is available. The MIT limits its interventions to adult patients hospitalized in non-critical care departments. Critical care patients are discussed weekly in a separate meeting with clinical
Figure 1 Flowchart activities multidisciplinary infectious diseases team.
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microbiologists and intensive care physicians. The pediatric department has a dedicated pediatric ID physician. The aim of this pilot study is to describe the type and acceptance rate of interventions provided by the MIT.
Methods A prospective, observational study was performed in a tertiary care, teaching hospital with 1062 beds. The MIT pharmacists registered every recommendation communicated by the MIT during 87 nonconsecutive days between October 2011 and May 2012. The following data were registered in a standardised case record form: date of MIT recommendation, hospitalisation ward, type of infection, and current antimicrobial treatment. Five types of recommendations can be distinguished: (1) initiating or changing an antimicrobial regimen; (2) additional
clinical investigations; (3) dosing adjustments; (4) switching from parenteral to oral formulations; and (5) discontinuing antimicrobials. The rationale for the recommendations and the specific antimicrobials involved were registered. Recommendations were scored as accepted when a physician implemented the recommendation(s) within 3 days after the communication. The acceptance rate was classified as ‘not documented’ in those cases where it was not possible to document this retrospectively (e.g. patient discharged or transferred to another health-care facility). The study was approved by the local Ethics Committee.
Results The MIT communicated 432 recommendations during 87 non-consecutive days in 293 patients The median age was 57 years (range: 16–91 years) and 169 (57.7%) were male.
Table 1 Classification of the recommendations provided by the MIT with acceptance rates
Classification of recommendation
Number of recommendations Accepted N (%) N (%)
Acceptance Not not documented accepted N (%) N (%)
(A) Additional clinical investigation Type of investigation Other* Microbiological culture CT scan Standard RX scan Therapeutic drug monitoring Standard echography Transoesophageal echography ID consultation Transthoracic echocardiography (B) Dosing adjustment Reason Subtherapeutic or toxic serum concentration Evidence-based guidelines Other{ renal impairment Type of adjustment Increase Reduction Same daily dose, other dosing regimen (C) Stop antimicrobial therapy Reason No indication to proceed Prolonged therapy Tentative (D) Switch parenteral to oral (E) Initiation antimicrobial therapy Reason Replacement Narrow spectrum Effectiveness Broaden spectrum Oral alternative Less side effects Addition Effectiveness Broaden spectrum Restart Reason unknown
137 (27%) 80 (58%) 43 (31%) 20 (15%) 13 (9%) 11 (8%) 9 (7%) 9 (7%) 8 (6%) 1 (1%) 42 (8%) 15 (36%) 15 (36%) 8 (19%) 4 (10%) 22 (52%) 11 (26%) 9 (21%) 104 (21%) 70 (67%) 25 (24%) 9 (9%) 39 (8%) 178 (36%) 113 (63%) 38 (34%) 30 (27%) 20 (18%) 19 (17%) 13 (12%) 26 (15%) 13 (50%) 13 (50%) 2 (1%) 2 (1%)
5 (4%) 2 (3%) 0 (0%) 1 (5%) 0 (0%) 0 (0%) 0 (0%) 2 (22%) 0 (0%) 0 (0%) 3 (7%) 0 (0%) 2 (13%) 1 (13%) 0 (0%) 2 (9%) 0 (0%) 1 (11%) 4 (4%) 4 (6%) 0 (0%) 0 (0%) 1 (3%) 11 (6%) 7 (6%) 1 (3%) 2 (7%) 1 (5%) 1 (5%) 1 (8%) 1 (4%) 0 (0%) 1 (8%) 0 (0%) 0 (0%)
100 (73%) 62 (78%) 32 (74%) 14 (70%) 10 (77%) 9 (82%) 6 (67%) 7 (78%) 5 (63%) 1 (100%) 35 (83%) 12 (80%) 12 (80%) 7 (88%) 4 (100%) 16 (73%) 11 (100%) 8 (89%) 85 (82%) 57 (81%) 22 (88%) 6 (67%) 30 (77%) 150 (84%) 94 (83%) 32 (84%) 26 (87%) 15 (75%) 17 (89%) 10 (77%) 23 (88%) 12 (92%) 11 (85%) 1 (50%) 2 (100%)
32 (2%) 16 (20%) 11 (26%) 5 (25%) 3 (23%) 2 (18%) 3 (33%) 0 (0%) 3 (38%) 0 (0%) 4 (10%) 3 (20%) 1 (7%) 0 (0%) 0 (0%) 4 (18%) 0 (0%) 0 (0%) 15 (14%) 9 (13%) 3 (12%) 3 (33%) 8 (21%) 17 (10%) 12 (11%) 5 (13%) 2 (7%) 4 (20%) 1 (5%) 2 (15%) 2 (8%) 1 (8%) 1 (8%) 1 (50%) 0 (0%)
Note: *Procalcitonin measurement (12 recommendations); nuclear magnetic resonance scan (6); bronchoalveolar lavage (4); polymerase chain reaction analysis (4); positron emission tomography (3), etc. { Different length of administration, increase of dose for penetration into sternum bone, increase of dose because of intermediate sensitivity of bacterial strain, increase of dose because of infection of vascular prosthesis, different dosing regimens because of parenteral administration in home setting, increase of dose because of high body weight, tentative.
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Skin or soft tissue infections (14%), respiratory tract infections (13%), infections without known focus (11%), abdominal infections (11%), and bone and joint infections, including prosthetic infections (8%), were most frequently involved. In 277 (64.1%) of the recommendations, the MIT proposed a modification in therapy or further clinical investigations which were accepted. In 84 (19.4%) of the recommendations, the MIT suggested to continue the actual therapy which was implemented. This resulted in a total acceptance rate of 83.5%. For the other recommendations, 57 (13.2%) were not implemented and for 14 (3.2%) implementation could not be documented. MIT recommendations originated from new electronically requested ID consultations (61%), current antimicrobial therapies provided by pharmacists (18%), follow-up of earlier requested ID consultations (12%), microbiological information provided by microbiologists (4%), current therapies provided by ID physicians (3%), and haematologists (2%). The electronic ID consultations were ordered by 30 medical disciplines, ranging from 1 to 24 (median: 7.5) requests per discipline. The majority of the recommendations were made for patients on the following wards: abdominal surgery (16.2%), gastroenterology (9.3%), thoracovascular surgery (7.9%), rehabilitation medicine (5.8%), and orthopaedics (5.0%). Some of the 432 recommendations consisted of multiple types of recommendations, which were taken into account individually in Table 1. This resulted in 500 individual recommendations. Recommendations were made to perform additional clinical investigation(s) [N5137 (27%)], to adjust a dose of an antimicrobial drug [N542 (8%)], to stop an antimicrobial drug [N5104 (21%)], to switch from a parenteral to an oral drug [N539 (8%)] and to initiate an antimicrobial drug [N5178 (36%)], with an acceptation rate of respectively 73.0%, 83.3%, 81.7%, 76.9%, and 84.0% (Table 1). Of the 178 initiated antimicrobials, 113 (63%) were a replacement of and 26 (15%) an addition to the current therapy. Within the accepted recommendations, vancomycin, piperacillin/tazobactam, and meropenem treatments were more frequently stopped versus initiated (respectively 31 versus 5, 21 versus 7, and 20 versus 14). Considering the administration route, parenteral therapies were more frequently stopped than initiated (148 versus 97). In general, treatments were more frequently discontinued instead of initiated (184 versus 152) after a MIT recommendation. This is not a likelihood but a frequency distribution as recommendations to continue treatments were more likely to be implemented.
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Discussion This study shows that an average of five recommendations per day was provided by the MIT, of which 83% were accepted. This acceptance rate is comparable with numbers in similar studies performed in the USA, Brazil, Singapore, and Australia, showing acceptance rates ranging from 64% to 80%.8–12 Remarkably, the number of recommendations seems slightly higher in our study. This could be the result of the inclusion of pharmacotherapeutic, as well as diagnostic recommendations, in contrast to the previously published reports. In the other studies, the AMT program was performed by ID physicians, together with clinical pharmacists, whereas only in one study, there was also participation of a clinical microbiologist (9). The numbers of beds ranged from 60 to 1596.8–12 Our recommendations cover a wide range of infection types, with a majority of skin or soft tissue infections, respiratory tract infections, infections without known focus, and abdominal infections. Some of these infections can be complicated and complex, requiring a long duration of therapy, a setting in which the advice of the MIT can be important. The majority (61%) of the recommendations originate from ID consultations. This may reflect the embedment of this clinical service within the hospital. A significant number (18%) of recommendations originate from therapies reviewed by clinical pharmacists. Pharmacists spend approximately 2 hours per day in analysing treatments with antifungals (with the exception of fluconazole), meropenem, piperacillin/ tazobactam, linezolid, tigecycline, vancomycin, teicoplanin, and antimicrobials with a high bioavailability that may be switched from parenteral to oral administration. Because this represents a significant workload each type of antimicrobial agent is reviewed only once a week. Data-mining software able to generate automated reports based on pharmaceutical, clinical, and microbiological data could have a time-saving effect.11 This should allow us to enhance the frequency of the actual antimicrobial agents and to evaluate additional antimicrobial agents. Furthermore, computer decision support systems could support physicians upon the initiation of a therapy.13,14 Such a system is already applied on the intensive care unit of our hospital.14 However, this was outside the scope of the current study. The number of recommendations originating from positive microbiological cultures provided by clinical microbiologists is small, because during the time period of the study, most of the positive cultures were directly discussed by the clinical microbiologists with the treating physicians outside the framework of the MIT. This is a direct consequence of the different
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organisation of the microbiology laboratory, where the results are generated early in the morning, in contrast with the MIT meetings which are held in the late afternoon. The majority (73%) of the recommendations focus on pharmacotherapy. All recommendations to reduce the dose of antimicrobials were accepted, while recommendations to increase the dose had a lower acceptance rate. Physicians seem to feel more confident with reducing doses considering compromised renal function or risk of side effects. They may not yet be fully aware of the concept of individualised antimicrobial therapy. This may require increasing doses, e.g. in infections with less sensitive strains, in patients with significant pharmacokinetic changes, such as increased distribution volume (burns, cirrhosis) or the phenomenon of augmented renal clearance in critically ill.15 Recommendations that propose a tentative stop of an antimicrobial therapy and an observation of the clinical evolution imply a greater degree of uncertainty for physicians which can explain the low acceptance rate in this setting. The acceptance rate to switch from a parenteral to an oral formulation (IV–PO switch) of the same antimicrobial is relatively low. An explanation could be that pharmacists’ only source to consider possible switches is the electronic medical record where clinical data that could support the medical decision to continue parenteral therapy (e.g. severe vomiting, diarrhea, not functional tube) were not always documented. The proportion of recommendations proposing an IV–PO switch is small, which could be the result of other and earlier initiatives towards physicians. Within the same hospital, we have reported high compliance with internal guidelines on IV–PO switch.16,17 These initiatives were developed outside the framework of the MIT, but were coordinated by the AMT. Recommendations to initiate an antimicrobial therapy have the highest overall acceptance rate with physicians. Most recommendations in this category propose to replace a current antimicrobial by an alternative. Most persuasive reasons to initiate an antimicrobial therapy were to enhance effectiveness, to narrow spectrum, and to allow a switch to oral therapy. The analysis of accepted recommendations suggests that the MIT was able to de-escalate therapies, to switch to oral antimicrobials, and to discontinue antimicrobials when applicable. About 17% of the recommendations focus on additional clinical investigations with an acceptance rate of 73%, which is lower compared to pharmacotherapy oriented recommendations, but comparable with a recently published similar study.18 The lower acceptance rate on diagnostic issues suggests that physicians more readily accept recommendations
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on pharmacotherapy as compared to critical reflections on their diagnostic path. This is also shown by the low uptake of performing transesophageal echocardiography in patients with Staphylococcus aureus bacteraemia. As a result of these data, patients with a Staphylococcus aureus bacteraemia are now prospectively followed during their hospital stay to ensure echocardiography screening for latent infective endocarditis.19 Establishing a culture of measurement and clinician feedback is an effective stewardship strategy.4,20 The effectiveness can be improved by the Feedback Intervention Theory through providing specific, frequent, and written suggestions for improvement.21 This was also applied by the MIT by documenting recommendations in the CPOE system and by additional communication by phone. Another strength of the MIT is that follow-up by the MIT is provided for patients with complex infections. This is strongly appreciated by the physicians. The multidisciplinary composition of the MIT reflects the recommendations in the literature.2,4,22 The MIT is directed by an infectious disease physician who is a respected authority which is a fundamental feature in marketing the MIT concept.23 Initially, the pharmacist reviewed only prolonged therapies (.10 days) of the target antimicrobial agents, which have changed over time to all treatments. Pre-authorization of restricted antimicrobial agents is not implemented in our hospital and only once a week, each type of antimicrobial agents is reviewed. The combination of these two factors indicates potential for further optimization. This will increase the workload, which can be in turn reduced by implementing automated reports. One study from a hospital in the USA with 513 beds described that software-generated antimicrobial therapy reports contain information on approximately 60–80 patient cases, resulting in about 20 cases daily after evaluation by a pharmacist. These cases are then reviewed together with an ID physician. Projecting this method to our hospital, this could generate 36 cases on a daily basis to discuss within the MIT.11 In order to support physicians during the diagnostic evaluation of the patient, some guidelines are now linked to the data of clinical chemistry (e.g. serum concentration levels of glycopeptide and aminoglycoside agents are linked to drug therapeutic monitoring guidelines) and microbiology (positive blood cultures with Staphylococcus aureus are linked to the Staphylococcus aureus bacteremia guideline). This pilot study has some limitations. Reasons to decline a recommendation were not assessed. Recent literature on antimicrobial stewardship focuses on the behaviour of individual prescribers. This could lead to understanding the barriers to and facilitators of
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behavioural change.24 This should be taken into account for further research. No statements can be made on the cost-effectiveness, patient safety, impact on morbidity, and mortality and local resistance patterns. Restricted antibiotics (e.g. vancomycin, piperacillin-tazobactam, and meropenem) were more frequently stopped than initiated and oral therapies were more frequently initiated compared with parenteral therapy. This suggests that the MIT can have a positive impact on antimicrobial expenditure. In the past, this was shown in our hospital for an IV–PO switch program.16 This is in line with documented positive impact of antimicrobial stewardship programs on antimicrobial expenditure and clinical outcome.8–12,25
Conclusion This prospective observational pilot study showed that the multidisciplinary infectious diseases team, as part of an antimicrobial stewardship program, formulated about five interventions a day for noncritically ill adult patients. Recommendations were communicated by phone and by notes in the electronic patient file resulting in high acceptance rates. Acceptance rates were higher for recommendations on pharmacotherapy as compared to diagnostic issues.
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Disclaimer Statements Funding None to declare.
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Conflicts of interest The authors declare that they have no conflict of interest.
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Ethics approval The study was approved by the local Ethics Committee.
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Acknowledgements We acknowledge the trainee hospital pharmacists Nele Clottens (PharmD), Ilse Vanlerberghe (PharmD), Mieke Van Tomme (PharmD), and the trainee infectious disease physicians Filip Moerman (MD), Sarah Temmerman (MD), and Bart Werbrouck (MD) for their contributions in the MIT activities. We acknowledge hospital pharmacist Annemie Somers (PharmD, PhD) for the critical remarks in analysing the data.
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